Detrimental effects of ticks ornithodoros maritimus on the growth of y

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Bosch M. & J. Figuerola 1999. Detrimental effects of ticks Ornithodoros maritimus

on the growth of Yellow-legged Gull Lrus michahellis chicks. Ardea 87: 83-89.

The effect of tick Ornithodoros (Alectorobius) maritimus larvae on the growth of Yellow-legged Gull Larus michahellis* chicks was studied at the Medes Islands col­ ony (NE Spain). Within broods, chicks infested by more larvae weighed less had a poorer body condition and a shorter wing length than their less infested siblings measured at a similar age. There were no differences in body measurements before tick infestation. Because mass and size of gull chicks are significant predictors of probability of fledging, the detrimental effect of 0. maritimus larvae on these param­ eters may affect the breeding success of Yellow-legged Gulls, and consequently their life-history and population dynamics.

Key words: Larus michahellis - Ornithodoros (Alectorobius) maritimus - chick growth B tick infestion
*FollTjerly known as Larus argentatus cachinnans (Voous 1973) or L. argentatus michahellis (Cramp 1983) or L. cachinnans michahellis (Del Hoyo et al. 1996)
‘Departament d’Ecologia, Universitat de Barcelona, Avda. Diagonal 645, E-08028

Barcelona, Spain. 2Department of Applied Biology, Estación Biologica de Doflana, CSIC, Avda. Maria Luisa s/n, B-41013 Sevilla, Spain.

Colonial birds can benefit from living in groups, e.g. by improving their defence against predators or their foraging efficiency (Wittenberger & Hunt

1985; Brown et al. 1990; Danchin & Wagner

1997), but this can also incur several costs. A fre­ quently reported cost is the greater risk of acquir­ ing ectoparasites, since close proximity of indi­ viduals facilitates host infestation (Wittenberger

& Hunt 1985; Brown & Brown 1986; Poulin

1991). The effects of ectoparasites on their hosts are diverse and include reduced host survival, fe­ cundity, quality of offspring, and breeding or mat­ ing success (see reviews in Møller et a!. 1990; Lehmann 1993). However, for some ectoparasite species no discernible effect has been detected (e.g. Rogers eta!. 1991; Tella et a!. 1995; Daw­ son & Bortolotti 1997).

Ornithodoros (Alectorobius) maritimus (Acari, Argasidae) is a soft tick that parasitises many spe cies of seabirds breeding in colonies from W. Eu­ rope and NW Africa (Hoogstraal et al. 1976). Like any tick, it is an obligate blood feeder para­ site (Olivier 1989). It may therefore affect host fit­ ness directly by taking blood and also indirectly by transmitting pathogens such as viruses (Chas­ tel 1988; Chastel et a!. 1993). Very few studies deal with the effects of this tick on the fitness of its hosts, so information is needed to assess any detrimental effect, and consequently to evaluate their possible impact on host population dynam­ ics. In this paper we report the effects of 0. marit­ imus larvae on chick growth of the Yellow-legged Gull Larus michahellis, a gull that breeds in large, dense colonies most of which are located in the Mediterranean basin (Beaubrun 1993).

The study was performed on the Medes Islands (42°00N, 3°13’E; NE Spain). These islands are a small calcareous archipelago of 20 ha, with one of the largest breeding colonies of Yellow-legged Gulls in the Mediterranean basin: ca. 13 500 pairs in 1993 (Bosch et al. 1994). This colony provided the first Spanish record of 0. maritimus, and a prehminary survey showed that around 90% of gull chicks were infested by larvae of this tick (Estrada-Pena et al. 1996). From 1992 to 1996 the colony was periodically culled by the regional na­ ture conservancy agency (DARP) because of the possible harmful effect of gulls (but see Bosch

1996). Culls were conducted on only some parts

of the colony, so it was possible to distinguish be­

tween unculled and culled areas (Bosch & Sol


During the breeding season of 1994, chicks from 42 nests in an unculled part of the colony were periodically measured and searched for 0. maritimus larvae from hatching to fledging or dy­ ing. Chicks were marked just after hatching with indelible ink and with metal rings from 15 days of age. Every two or three days, body mass and lengths of wing, bill and tarsus were recorded, and the number of 0. maritimus larvae on each chick was counted visually and by palpation of skin when body parts where covered with feathers (Danchin 1992; Boulinier & Danchin l996. All the parts of the chicks were systematically and exhaustively examined for ticks.

The effects of tick infestation on chick growth

were analysed by comparing measurements of siblings with different infestation levels. For each brood we identified the most infected chick and the least infected chick measured at a similar age (in all cases, 2 or less days of difference). The ranking of chicks according to infestation proved reliable when compared with the ranking of the same brood at least five days before (Kappa index

0.85, Z = 2.03, df= 11, P = 0.04, Fleiss 1981).

Normal approximation to the Wilcoxon Paired- Sample test (Z distribution) (Zar 1996) was used to compare the measurements obtained for each

pair of siblings in the last control obtained for both individuals, since data were not normally distributed. Only 12 of the 42 broods studied could be included in the analyses because in the remaining broods only one of the chicks hatched or survived more than one week after hatching, or because the whole brood was uninfected. Since all the chicks in each brood were captured, meas­ ured and checked for parasites with a same peri­ odicity, any possible effect of investigator distur­ bance on chick development was assumed to af­ fect equally both groups of siblings (most and least infected).

To test for possible differences in chick growth unrelated to parasite infestation, body measurements were also compared by using data from the same pairs of individuals on the last con­ trol before reporting the presence of parasites on any of the siblings. Two pairs were not available for these analyses because at least one of the chicks was infested by ticks from the first control after hatching.

By comparing data obtained from siblings

with different levels of parasites we solved the non-independence of data obtained from the same broods, so controlling for any parental effect on chick measurements (Merino & Potti 1995; Alves

1997). A possible association between intensity of parasites and hatching order within a brood was investigated using the Fisher Exact test, to estab­ lish whether most infected siblings systematically hatched before or after least infected siblings.

Finally, to simultaneously control for the ef­ fect of parasites and hatching order, we calculated growth rates for chicks measured at least twice during the lineal phase of growth (between 15 and

30 days in this population; M. Bosch & D. Oro

unpubl. data). Measurements were standardised to account for inter-brood differences by express­ ing chick growth with respect to mean brood growth. Two-way ANOVA were calculated on these scores to test the effects of hatching order and parasite load on growth rate. In this case data was not available for one brood last measured at 7 days of age, so sample size was reduced to 22 in­ dividuals of 11 different broods. Body condition

was not included in these analyses because it was a character derived from other two morphological parameters, and it is not warranted to assume a period of lineal increase in this variable.

Most and least infested groups differed by a factor of three in the intensity of their infestations (4.3 ±

4.9 vs 13.9 4: 10.3 ticks per chick; Wilcoxon pai­

red-sampl& test, Z = 3.10, n = 12, P = 0.002).

Chicks with more ticks grew smaller wings (Z =

2.223, n = 12, P = 0.03), weighted less (Z= 2.51, ii = 12, P = 0.01) and were in a poorer body con­ dition (Z = 2.98, n = 12, P = 0.003) than least in­ fested individuals at the time of measurement (Table 1). However, no differences were found in

either bill (Z = 1.42, n = 11, n.s) or tarsus length (Z = 0.55, n = 12, n.s). The differences in size were not explained by differences in the age of siblings, since the age when chicks were meas­ ured did not differ significantly between siblings (Z= 0.35, n = 12, n.s). Furthermore, no significant relationship was detected between the hatching order of chicks and tick abundance (Fisher exact test, n.s.).

Before infestation by 0. maritimus no differ­ ences were detected for any of the characters be­ tween the most infected and least infected sib­ lings (bill: Z = 0.46, ii = 10, n.s.; body condition: Z= 0.97, n = 10, n.s.; tarsus: Z= 0.25, n = 10, n.s.; mass: Z = 0.53, n = 10, n.s.; wing: Z = 0.34, n =

10, n.s.). Once again no differences in the age of measurement occurred between either group of siblings (Z= 0.00, n = 10, n.s.).

Table 1. Measurements of the most and least infested sibling chicks on the date of last control and on the tast control beforedetection ofticks on any ofthe siblings. Mean ± SD and number of broods analysed are reported for each variable.
Last control Last uninfected control






















63.5 ± 9.6

62.4 ± 11.9


35.3 ± 11.6

35.5 ± 12.1























Table 2. Chick growth rate (expressed in mm da3r1 and g day-1)according to hatching order and parasite rank during thelineal phase ofchick growth(between 15 and 30days).Valuesfor each chick have been standardized by taking away the mean brood growthrate. Mean ± SD and numberofchicks analysed are reported for each variable.

Hatching order

Parasite rank
















-0.01 ±0.19


-1.50± 1.83





0.01 ±0.19


1.50± 1.83




-3.71 ± 4.08

-0.05 ± 0.07

-0.00 ± 0.19

-0.67 ± 1.40


Although we did not detect differences in hatching order between more and less infested chicks, given our small sample size and conse­ queritly small power to detect such kind of differ­ ences, we controlled for the possible effects of tick load and hatching Qrder on growth rate in a two-way ANOVA. A significant effect of parasite load on tarsus growth rate was detected (F118 =

5.59, P = 0.03), in addition to the previously re­

ported effects on body mass (F118 = 17.63, P

0.0005) and wing length (F118 = 9.03, P = 0.008; Table 2). Again, no effects of parasite load on bill growth rate were detected (F118 = 0.93, n.s.). Al­ though studying the effects of hatching order was nOt among the objectives of this study, we found a significant effect on tarsus growth (F118 = 5.52, P

0.03) but no effect for the other variables (body

mass. F118 = 0.89. n.s.: bill. F118 = 0.62. n.s.:

wing, F118 = 1.32, n.s.).


Several studies have shown that nestlings are very susceptible to ectoparasites, resulting in a de­ crease of their body size and condition (Arendt

1985; Brown & Brown 1986; Eeva et al. 1994; MØller et al. 1994; Merino & Potti 1995; 1996; Christe et a!. 1996; Dufva & Allander 1996; Alves

1997; Allander 1998, Hurtrez-Boussès eta!. 1998)

or a lower fledging success (Brown & Brown

1986; Eeva eta!. 1994; Møller 1990; 1994; Menno

& Potti 1995; 1996). In the present study, Yellow- legged Gull chicks with high levels of 0. mariti­ mus larvae were lighter mass, had a poorer body condition and a smaller wing length than those least infested. Such differences in body measure­ ments did not occur before any parasitism was de­ tected, so were probably due to the infestation by ticks. Since comparisons were performed be­ tween siblings within broods, no parental effect on the size and condition of chicks from different broods (Bolton 1991) could bias these results. Be­ cause laying order and sequence of hatching wit­ hin a clutch can affect growth and body condition of gull chicks (Parsons 1970; Barrett & Runde

1980), the smaller size and leaner body condition of the most infected siblings could have been also due to having hatched later than those least in­ fected. However this hypothesis is rejected be­ cause tick intensity was not related with the hatching order of siblings, and the differences re­ mained significant even when controlling for this variable.

The detrimental effect of 0. maritimus could arise as a direct or indirect consequence of its haematophagous habits. A direct effect would be because consumption of blood from hosts can im­ pose energetic costs on hosts (Møller et a!. 1994). In this way, Chastel eta!. (1987) noted that hyper­ infestation by 0. maritimus might lead to enough subacute or acute anaemia to produce chick death. Indirect effects would be through pathogen trans­ mission. such as viruses or haematozoa which, in turn, could also cause a deteriorate body condi­ tion of gulls (Bosch et a!. 1997). More than nine viruses have been isolated from 0. maritimus, some of which are pathogenic for birds (Hoog­ straal et a!. 1976; Chastel 1988; Chastel et a!.

1993). The transmission of haematozoa by this

tick species is still unknown, but seems probable since it has been found for another species of the same genus (Bennett et a!. 1992). In addition, it has been reported that 0. maritimus bites cause severe cutaneous irritation and sometimes febrile reactions (see references in Chastel 1988) that also could affect the body condition of chicks.

It has been suggested that ticks may affect the breeding success and, consequently, the life-his­ tory and population dynamics of colonial seabirds (Duffy 1983; Boulinier & Danchin 1996). The det­ rimental effect of 0. maritimus on growth of gull chicks might affect the fledging success of in­ fested chicks, since mass and size of gull chicks are significant predictors of their probability of fledging (Parsons 1970; Bolton 1991). In such case, given the high percentage of chicks infected by this tick in the Medes Islands colony (more than 90% in a preliminary survey; Estrada-Pefla et a!. 1996) a potential effect of 0. maritimus on the breeding success and dynamics of this colony should not be underestimated.

We thank A. Galdeano, K. Bosch-Vilalta, K. Bosch­ Mestres, T. Orantes, N. Pocino, I. PinS and J. M. 5cr- rano for their help in the field work; Port Autónom de Barcelona and Servei de Vigilància de les Illes Medes for their logistic support in the field; Dr A. Estrada­ Pena for his help and advice in the identification of 0. maritimus larvae. R. Cryford for improving the English text. Drs F. J. Cantos, M. Zabala, C. J. Camphuysen and one anonymous referee for their helpful comments on the manuscrip4


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Het leven in kolonies heeft een flunk aantal voordelen, zoals de mogelijkheid tot collectieve verdediging tegen predatoren en een verhoging van de efficientie bij bet foerageren. Er zijn echter ook kosten. Zo lopen dicht opeen nestelende vogels een groter risico om met ecto­ parasieten besmet te raken. Parasieten zoals veerluizen en teken hebben allerlei nadelige effecten voor de gast­ beer, uiteenlopend van een verhoogde sterfte van de gastheer, via een verminderde vruchtbaarheid, tot bij­ voorbeeld een geringere vitaliteit van de kuikens. Over het algemeen wordt aangenomen: hoe meer parasieten hoe groter het nadelige effect, en voorjonge vogels zul­ len de gevolgen al snel groter zijn dan voor oudere die­ ren. De effecten van ectoparasieten zijn echter nog niet vaak in detail bekeken. Ornithodoros (Alectorobius) maritimus is een teek die in veel zeevogelkolonies in West-Europa en Noordwest-Afrika wordt aangetroffen. Zoals vrijwel aPe teken leeft deze parasiet van het bloed van de gastheer. Behalve een direct nadeel (het aftappen van bloed) levert deze parasiet ook risico’s op door de overdracht van bijvoorbeeld virusziekten. In dit artikel wordt het effect van een tekenbesmetting op de groei van kuikens onderzocht bij Geelpootzilver­ meeuwen Lw-us michahellis in een kolonie op de Me- des Eilanden (NO Spanje). Voorafgaande aan de be­ smetting met teken bestonden er geen meetbare ver

schillen tussen de verschillende groepen onderzochte nest. De negatieve effecten op de groei hingen af van meeuwenkuikens. Kuikens die met teken besmet raak- de mate van besmetting met teken.

ten, bleven achter in de groei (lager gewicht, langza­

mere groei van de vleugels) dan een kuikens waarbij

geen teken werden gevonden. Deze onderlinge ver-

schillen waren zelfs zichtbaar bij kuikens van hetzelfde

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